Coprophilous myxomycetes of Brazil: first report

Maria de Fatima de Andrade Bezerra 1, Wendell Medrado Teófilo da Silva2, Laise de Holanda Cavalcanti3 1Programa de Pós-graduação em Biologia de Fungos, Universidade Federal de Pernambuco (UFPE). Av. Prof. Moraes Rego s/n, Cidade Universitária, Recife-PE, 50.560-901, 2Mestrando em Biologia de Fungos, UFPE. 3Laboratório de Myxomycetes, Departamento de Botânica, Centro de Ciências Biológicas, UFPE 8 0 0 2

Myxomycetes coprófilos de Brasil: primer reporte , 7 3 -

Resumen. El propósito de este estudio fue identificar especies de mixomicetos que 9 2

esporulan sobre heces de animales en Brasil. Se prepararon cámaras húmedas a partir de : 7 2

muestras de heces del “tapeti”, conejo brasileño (Sylvilagus brasiliensis) y de caballo (Equus A Í

caballus), recolectadas en 14 excursiones realizadas en el Parque Nacional Serra de G O

Itabaiana, Sergipe. El pH inicial de los cultivos en los que se registró esporulación osciló entre L O C

(3,8) 4,15 y 4,64 (5,55). Se obtuvieron 52 especímenes (62 cámaras húmedas, 34% I M positivas), con diez morfoespecies, distribuidas en las familias Cribrariaceae (Cribraria 4 E D

especies), Physaraceae (Physarum 2 especies), Stemonitaceae (Comatricha 1 especie) y A

Trichiaceae (Arcyria 1 especie, Hemitrichia 1 especie, Metatrichia 1 especie). Los N A C especímenes del material estudiado fueron depositados en el Herbário UFP. Todas las I X

especies son nuevos registros de mixomicetos coprófilos para Brasil. Los registros de Cribraria E M

cancellata, C. microcarpa, Metatrichia vesparia y Physarum roseum constituyen las primeras A T S referencias a nivel mundial de estas especies en heces de herbívoros. Cribraria mirabilis se I V E

reporta por primera vez para Brasil. R

Palabras clave: Conejo, caballo, heces.

/

o c

Abstract. The aim of this work was to identify the species of myxomycetes associated with the i x é

dung of wild and domestic animals in Brazil. Moist chamber cultures were prepared with M

n e

samples of the dung of the wild Brazilian rabbit (Sylvilagus brasiliensis) or horses (Equus a s e

caballus) collected during 14 field trips to the Serra de Itabaiana National Park, Sergipe State. r p m

Initial culture pH ranged from (3.8) 4.15 –4.64 (5.55). Fifty two specimens from 62 cultures I

. a (34% positivity) were obtained, representing ten morphospecies, distributed in the families í g o l

Cribrariaceae (Cribraria cancellata, C. microcarpa, C. violacea and Cribraria sp.), Physaraceae o c i M

(Physarum cinereum and P. roseum), Stemonitaceae (Comatricha aff. mirabilis) and e d Trichiaceae (Arcyria cinerea, Hemitrichia minor and Metatrichia vesparia). All species are new a n a

records of coprophilous myxomycetes in Brazil. The reports of C. cancellata, C. microcarpa, c i x M. vesparia and P. roseum are the first records in the world of these species on the dung of e M

a

herbivores. This is the first citation of C. mirabilis for Brazil. t s i v

Key words: Rabbit, horse, dung. e R

8 0 0 2

Received 3 March 2006; accepted 13 February 2008.

Recibido 3 de marzo 2006 ; aceptado 13 de febrero 2008. ©

Autor para correspondencia: M. F. Andrade Bezerra L

[email protected] A N I G I R O the three subclasses, indicating that the capacity to occupy The samples were collected in the Serra de Itabaiana National Cribrariaceae L A N Introduction I

this microhabitat is present in different evolutionary lines. Park – PNSI, SE (10º 40' 52"S, 37º 25' 15"W, 4,389.76 ha, Cribraria cancellata (Batsch) Nann.-Bremek., Nederlandse G I R

Characteristics that support endocoprophilia are not 180–670m alt.), in areas of savanna (ca. 250 m alt.) and in Myxomyceten: 92. 1975. O Denizens of animal excrement are categorized as fimicolous present in the sporocarps of myxomycetes Ing [13] and open fields on the summit of the mountain. According to the Cosmopolitan, with records for Amazonas, Bahia, Ceará, or coprophilous, encompassing species found at distinct Eliasson & Keller [10] question whether these species are in availability of material in the field, 62 moist-chambers were Paraíba, Ceará, Paraíba, Paraná, Pernambuco, Piauí, Paraná, levels of degradation of the substrate. Denizens of the primary fact endocoprophilous or if the members of this class inhabit prepared (51 with rabbit feces and 11 with horse feces). Rio de Janeiro, Roraima and São Paulo [6; 17; 22]. This stage (fimicolous) occupy a substrate where fermentation is feces secondarily, a situation they consider more probable. Collections were made during 14 monthly excursions. After species is very common and widely distributed in the world most active, while later denizens (coprophilous) of the Nevertheless, works which document the occurrence of having the initial pH of the cultures recorded, the cultures and in Brazil, being frequently found on rotting wood, acting secondary stage occupy a substrate characterized by the lack myxomycetes on feces of rabbit fed in a lab on Medicago were maintained at ambient light and temperature (± 28ºC) like a lignicolous species. This is the first record, at a global of fermentation [20, 3]. A third group, the subcoprophilous sativa L. [27, 2], and that which obtained fructification of levels and observed for a period of at least three to a maximum level, of this species as fimicolous [10, 19]. Rabbit feces in species, was proposed to indicate the species which need fecal myxomycetes from a suspension of mite feces [14], prove of six months. The cultures were considered positive when the which sporocarps of C. cancellata appeared were collected at material for nutrition, but do not develop directly on it, as that at least some species can behave as endocoprophiles. appearance of plasmodia and/or sporocarps was observed. the end of the dry season (April), in an area of savanna of the happens in land fertilized with manure [20]. In Brazil, several works refer to coprophilous Ten moist-chambers that had been set up with rabbit feces, PNSI. During four months, only plasmodial tracks were The first records on the development and sporulation microorganisms [4, 26, 23, 1], however, until now no study collected on different excursions and in which aborted observed in a moist-chamber that, re-humidified after nine of myxomycetes on feces of herbivores date to the 19th has included the myxomycetes. Cavalcanti et al. [7], despite plasmodia had been recorded, were maintained dried for months of dehydration, developed typical sporangia in a little

Century, from studies done in Europe [11]. Since then, several not treating the fimicolous species, comment on the eight–12 months, after which time they were re-hydrated and more than seven weeks of cultivation. t r o p

workers have mentioned the presence of these organisms on fertilization of nurseries with chicken manure which observed for three months. Identification of species was Examined material: BRAZIL. Sergipe: Areia e r

t s r

excrement of different animals, domesticated or wild, on produced abundant fructification of Fuligo cinerea based on [12, 16, 18, 19]. Representative samples of the Branca, Serra de Itabaiana National Park, on feces of i f

: l i

almost all continents. (Schwein.) Morgan, to the point of killed tomato seedlings, studied material were deposited in the myxomycetes Sylvilagus brasiliensis L., 03/IX/2004, Bezerra, MFA 1121 z a r B

In the first comprehensive treatment of fimicolous and could be characterized as subcoprophilous. collection of the Herbarium UFP, Department of Botany, (UFP). f o

myxomycetes [11], 80 species were listed, occurring in In consideration of the important role of Federal University of Pernambuco. s e t e

Europe, Asia, Africa and the Americas; beyond providing a coprophilous microorganisms in the functioning of Cribraria microcarpa (Schrad.) Pers., Syn. Meth. Fung.: 190. c y m 8 general idea about species which can occur on feces of ecosystems, participating in the decomposition and 1801, emend. Nann.-Bremek., Proc. Kon. Ned. Akad. o x 0 y 0 m 2 herbivores, the authors discussed certain taxa which can be mineralization of herbivore feces or aiding the nutrition of Results and discussion Wetensch., C. 69 (3): 340. 1966.

s , u 7 o l 2

considered predominantly or exclusively fimicolous. After 20 coprophagous insects [2] and, at the same time, with the intent Cosmopolitan, with records for Bahia, Pernambuco, Piauí, i

h A p Í o

G years, a second treatment was published [10], adding 22 of widening knowledge about Brazilian myxobiota, the first Ten morphospecies were recorded, distributed among six and São Paulo states [6, 17]. This species is common in the r O p L o

records of coprophilous myxomycetes for the country are C O species to the list of myxomycetes that occupy this genera and four families, representing the subclasses PNSI, occurring in different seasons of the year, in diverse

. C l I a

M microhabitat. Currently, 23 genera and about 100 species that presented in this work. Stemonitomycetidae and Myxogastromycetidae. All of the microhabitats, behaving commonly as a lignicolous slime t

e

E . D F

sporulate on animal excrement are known, corresponding to a species constitute new records of coprophilous myxomycetes mold, yet also developing on dead leaves of members of the . A M

N little more than 10% of the species recognized for the class for Brazil, although they have already been recorded as Arecaceae and Bromeliaceae and living stems of members of , A a r C r I

Material and methods e X

Myxomycetes [15]. Considering that many of these species occurring in other microhabitats in other parts of the country, the Apocynaceae. Numerous sporocarps developed on horse z E e M B

also occur on other substrates and are only occasionally found with the exception of Comatricha mirabilis K. Benj. & feces collected during the dry season (October) on the e A d T S a I on feces of herbivores, Eliasson & Keller [10] concluded that Moist-chamber cultures were prepared from samples of feces Poitras. The three species in the Trichiaceae and the family mountain summit (659 m alt.), four to six weeks after r d V n E

R only 15 of them could be treated as truly fimicolous, in the of horse (Equus caballus L.) and of tapeti, the Brazilian rabbit Stemonitaceae also constitute new records for the state of placement in moist-chambers. While less abundant, A sense that records of them have, until now, been restricted to (Sylvilagus brasiliensis L.). Tapeti is a species in the Sergipe. sporulation after seven weeks of culture was also recorded on this microhabitat. It is worth pointing out that such species Leporidae considered threatened with extinction; it inhabits rabbit feces collected during the dry season (February) in the belong to three of the six orders of myxomycetes and two of fields, forests and savannas, and eats fruits, shoots and leaves. savanna. This is the first record for this species, on a global 1 0 3 3 level, on the feces of herbivores [10, 19]. 07/XI/2002, Bezerra, MFA 939 (UFP); idem, 31/VIII/2002, spores. Based on the information accumulated in the last 40 Examined material: BRAZIL. Sergipe: Areia L A N I

Examined material: BRAZIL. Sergipe: Areia Bezerra, MFA 940 (UFP); idem, 26/XII/2002, Bezerra, MFA years on reproductive systems and biology of the Branca, Serra de Itabaiana National Park, on feces of G I R

Branca, Serra de Itabaiana National Park, on feces of 941 (UFP); idem, 10/XII/2002, Bezerra, MFA 949 (UFP); myxomycetes, some authors are of the opinion that many Sylvilagus brasiliensis L., 26/III/2003, Bezerra, MFA 324 O Sylvilagus brasiliensis L 05/IV/2003, Bezerra, MFA 323 idem, 25/I/2003, Bezerra, MFA 964 (UFP). species defined in morphological terms constitute in reality (UFP); idem, 28/III/2003, Bezerra, MFA 325 (UFP); idem, (UFP); idem, on feces of Equus caballus L., 02/XII/2002, species complexes that consist of various combinations of 30/III/2003, Bezerra, MFA 326 (UFP); idem, 05/IV/2003, Bezerra, MFA 929 (UFP); idem, 25/XI/2002, Bezerra, MFA Cribraria sp. biological species and multiple apomyctic lines [9]. As such, Bezerra, MFA 327 (UFP); idem, 18/IV/2003, Bezerra, MFA 930 (UFP). In one of the four moist-chambers prepared with rabbit feces many commonly accepted morphospecies would be only 328 (UFP); idem, 06/IV/2003, Bezerra, MFA 329 - B (UFP); collected at the end of the dry season (March), sporangia morphotypic variations, differing from the principal taxon in idem, 27/IV/2003, Bezerra, MFA 1036 (UFP). Cribraria violacea Rex, Proc. Acad. Nat. Sci. Philadelphia developed that were similar in coloration to those of C. only a few genes, or biotypic variations adapted to a specific Physaraceae 43: 393. 1891. violacea but with globose sporotheca and that did not possess part of the microhabitat [9, 25]. The authors who support this Physarum cinereum (Batsch) Pers., Neues Mag. Bot. 1: 89. Cosmopolitan, recorded in Paraíba, Pernambuco, Piauí, Rio the deep calyculus typical of this species. In all seven opinion recommend that new species should only be 1794. Grande do Norte, and São Paulo states [6, 17]. This species is collections obtained, sporulated in different seasons, the described after extensive study, based on several collections Cosmopolitan, with records from Amazonas, Bahia, poorly recorded in Brazil, though it has been noted from many sporocarps tended to be smaller (0.7–0.8 mm tall), the stipes from different locations. Based on such considerations, the Pernambuco, Minas Gerais, and Santa Catarina states [6; 17; different regions of the country. All 17 specimens obtained in are shorter and less thin (0.50–0.60 mm long, 72.2–91.2 µm specimens Bezerra MFA 324, Bezerra MFA 325, Bezerra MFA 22]. The only specimen of Physarum cinereum obtained in the the PNSI sporulated in the same moist-chamber, on rabbit wide at the base, and 11.4–26.6 µm wide at the apex), the 326, Bezerra MFA 327, Bezerra 328, Bezerra MFA 329 – B, PNSI developed on rabbit feces collected in savanna in the

feces from the savanna collected at the end of the dry season spores tend to have greater diameter (7.65–9.18 µm) and the and Bezerra MFA 1036 were identified only to the level of rainy season (August), after a little more than four weeks of t r o p

(April). On different occasions, they developed one to 15 peridial net has distinct characteristics (Figure 1a-c). genus, awaiting new data for the description of a probable cultivation, is formed of abundant sporocarps with the typical e r

t s r

sporocarps with the typical characteristics of the species, Cribraria violacea and Cribraria sp. developed on rabbit new species. characteristics of the species. This is the first citation of this i f

: l i

starting sporulation four months and two weeks after being set feces, collected in a 100 m² area; however, the latter was species for the state of Sergipe. z a r B

up in the moist-chambers, and going through a 16 successive obtained 11 months after the collection of the former species. Examined material: BRAZIL. Sergipe: Areia f o

fructifications in more than five months. In the same culture, Beyond the morphological characteristics, there also existed Branca, Serra de Itabaiana National Park, on feces of s e t e

simultaneous or alternate development of M. vesparia was differences in the timing of sporulation. Cribraria sp. Sylvilagus brasiliensis L., 20/IX/2002, Bezerra, MFA 934 c y m 8 observed. Cribraria violacea is the only representative of the developed on substrates considerably less degraded by the (UFP). o x 0 y 0 m 2 Cribrariaceae with records from the feces of herbivorous passage of time as fructification started after ten days, much

s , u 7 o l 2

animals [10]. less than recorded for C. violacea (134 days), forming four to Physarum roseum Berk. & Broome, J. Linn. Soc., Bot. 14: i

h A p Í o

G Examined material: BRAZIL. Sergipe: Areia 12 sporocarps every one to ten days, during a period lasting 84. 1873. r O p L o C

O Branca, Serra de Itabaiana National Park, on feces of for six weeks. Sporocarps developed on all surfaces of the In Brazil, P. roseum has a restricted distribution, recorded

. C l I a

M Sylvilagus brasiliensis L., 12/I/2003, Bezerra, MFA 94 substrate, while C. violacea preferentially sporulated on the only from Pernambuco and São Paulo states, being associated t

e

E . D F

(UFP); idem, 19/I/2003, Bezerra, MFA 95 (UFP); idem, filter paper. only with humid forest areas in the Northeast and Southeast, . A M

N 29/I/2003, Bezerra, MFA 96 (UFP); idem, 01/XI/2002, Among the 42 species included in this genus, only C. as a foliicolous or corticolous slime mold [6, 17]. In the first , A a r C r I e X

Bezerra, MFA 894 – B (UFP); idem, 08/XI/2002, Bezerra, costata Dhillon & Nann. Bremek., C. elegans Berk. & M. A. record for the state of Sergipe, this species was isolated in z E e M B

MFA 895 - A (UFP); idem, 01/XII/2002, Bezerra, MFA 896 Curtis, C. paucicostata Nann.-Bremek., C. violacea Rex, C. substrate obtained from savanna vegetation. This species is e A d T S a I (UFP); idem, 18/XI/2002, Bezerra, MFA 897 (UFP); idem, lepida Meyl., C. purpurea Schrad., C. zonatispora Lado, easily recognized by its pinkish coloration and only r d V n E

R 23/XI/2002, Bezerra, MFA 898 (UFP); idem, 17/IV/2002, Mosquera & Beltrán-Tej., and C. fragilis Lado & Estrada- Physarum pulcherrimum Berk. & Ravenel has similar A Bezerra, MFA 899 (UFP); idem, 21/XI/2002, Bezerra, MFA Torres have a coloration similar to the studied specimens, but Figure 1. Cribraria sp. 1a. Sporocarps on rabbit excrements coloration, differing by the calcareous pedicel and columella (Sylvilagus brasiliensis L.); 1b. Sporocarp in optic 910 (UFP); idem, 18/XII/2002, Bezerra, MFA 911 (UFP); all of these differ in the other characters of taxonomic value, microscopy; 1c. Detail of the peridial net. Scales: 1a. = 0,4 that are absent in P. roseum [12]. Only one specimen, with the mm; 1b = 50 µm; 1c =10 µm. idem, 23/X/2002, Bezerra, MFA 938 (UFP); idem, particularly in those associated with the calyculus and the typical characteristics of the species, was obtained in the 3 2 3 3 PNSI, developing after 12 weeks of cultivation, from a description for C. mirabilis [5] except in the small diameter of Examined material: BRAZIL. Sergipe: Areia Sylvilagus brasiliensis L., 08/XI/2002, Bezerra, MFA 895 L A N I

plasmodium of blood-red color. In one of the moist-chambers the spores. In describing the new taxon, the authors compared Branca, Serra de Itabaiana National Park, on feces of (UFP); idem, 01/IX/2002, Bezerra, MFA 959 (UFP); idem, G I R

prepared with rabbit feces collected during the dry season it with C. rispaudii which possesses spores 9 µm in diam. or Sylvilagus brasiliensis L., 24/X/2002, Bezerra, MFA 1098 08/XI/2002, Bezerra, MFA 881 (UFP); idem, 09/VI/2002, O (January) in savanna areas, a plasmodium of the same less and a more reticulate capillitium. The six specimens (UFP); idem, 24/IX/2002, Bezerra, MFA s/n; idem, Bezerra, MFA 1102 (UFP); idem, 01/XI/2002, Bezerra, MFA coloration, typical of the species, was observed for some obtained at the PNSI developed in different moist-chambers, 19/I/2003, Bezerra, MFA s/n. 894 - A (UFP); idem, 28/XI/2002, Bezerra, MFA 880 (UFP); weeks, but it did not sporulate. This is the first record, on a prepared with rabbit feces from the savanna, collected during idem, 31/VII/2003, Bezerra, MFA 1082 - B (UFP); idem, global level, of the occurrence of P. roseum on the feces of the dry season (January, November) and in the rainy season Metatrichia vesparia (Batsch) Nann.-Bremek. ex G. W. 16/VIII/2003, Bezerra, MFA 1122 (UFP); idem, herbivores. (May). The sporocarps developed after three to 20 weeks of Martin & Alexop., Myxomycetes: 143. 1969. 26/VIII/2003, Bezerra, MFA 1123 (UFP). Examined material: BRAZIL. Sergipe: Areia cultivation, producing between two and 17 sporangia per Cosmopolitan, with records for all the regions of Brazil, Branca, Serra de Itabaiana National Park, on feces of culture; in the material from the seventh and ninth harvests, except the Central-West [6, 12, 17, 22]. In the PNSI, Hemitrichia minor G. Lister, J. Bot. 49: 62.1911. Sylvilagus brasiliensis L., 22/IV/2003, Bezerra, MFA 932 sporulation happened on two or three times in the same moist- exemplars of this species were obtained in moist-chambers Recorded in Pernambuco and Rio Grande do Norte states [6]. (UFP). chamber, with a minimum time of three weeks of culture. prepared with rabbit feces from the savanna collected at the This species is included in the list of coprophilous Physarum roseum and Metatrichia vesparia were found beginning of the rainy season (April, May). Metatrichia myxomycetes [10], yet it has also been recorded in other Stemonitaceae associated with this species. vesparia sporulated on six different occasions in the same microhabitats, such as bark and wood, which would cause it to Comatricha mirabilis R. K. Benj. & Poitras, Mycologia Examined material: BRAZIL. Sergipe: Areia moist-chamber on material collected at the start of the rains be regarded as corticolous and lignicolous [8]. In the PNSI, H.

42(4): 515. 1950. Branca, Serra de Itabaiana National Park, on feces of (April); the first sporulation occurring at two months of minor was recorded in the savanna area, sporulating in the t r o p

This is the first record of this species for Brazil. The type Sylvilagus brasiliensis L., 18/XII/2002, Bezerra, MFA 296 cultivation and nine sporocarps were formed at intervals of same moist-chamber on rabbit feces collected at the end of the e r

t s r

material of C. mirabilis sporulated in a moist-chamber (UFP); idem, 01/IV/2003, Bezerra, MFA 302 (UFP); idem, one, three, or 12 weeks, for more than five months. Two of the dry season (March), after 22 and 34 days, where the genus i f

: l i

prepared with goat feces, collected in the American state of 16/IV/2003, Bezerra, MFA 322 (UFP); idem, 12/I/2003, five moist-chambers prepared with material collected during Cribraria was also represented. In each case, the z a r B

Illinois [5]. In describing the new species, the authors Bezerra, MFA s/n; idem, 18/I/2003, Bezerra, MFA 883 (UFP); the rainy season (May) were positive, one of them developing fructifications were scarce, consisting of two to four f o

commented that the sporocarp characters are completely idem, 31/VII/2003, Bezerra, MFA 1082 - A (UFP). sporocarps of M. vesparia after 11 weeks of cultivation; when sporangia. s e t e

different from those of C. cylindrica (Bilgram) T. Macbr. substrate material submitted to eight months of dehydration Examined material: BRAZIL. Sergipe: Areia c y m 8 (=Paradiachea cylindrica (Bilgram) Hertel), C. rispaudii Trichiaceae was re-hydrated again, nine sporocarps of this species were Branca, Serra de Itabaiana National Park, on feces of o x 0 y 0 m 2 Hagelst. (=P. rispaudii (Hagelst.) Hertel) and C. dictyospora Arcyria cinerea (Bull.) Pers., Syn. Meth. Fung.: 184. 1801. observed within a little more than three weeks of cultivation. Sylvilagus brasiliensis L., 06/IV/2003, Bezerra, MFA 329 - A

s , u 7 o l 2

L. F. Celak. (nomen dubium, due to the lack of type material), Cosmopolitan, with a known distribution in all regions of The second moist-chamber, observed during six months, did (UFP); idem, 18/IV/2003, Bezerra, MFA 330 (UFP). i

h A p Í o

G the only species of the genus that also have reticulate spores. Brazil, except the Central-West [6, 17, 22]. This is one of the not produce any fructifications. However, following r O p L o )

º

In the material from the PNSI, the sporangia are erect, brown, dehydration for a period of five months, sporocarps of M. C O most common and widely distributed species of n

. (

C 12 l I s a e

M Prepared 1.0–1.2 mm tall, with short sporotheca – cylindrical to ovoid; myxomycetes, occurring as much in the tropics as in vesparia were observed on the substrate two weeks after r t

u 10 e

t Positive

E l . u D F

c

with a circular, brown hypothallus, a portion of the pedicel temperate or cold regions, developing on a great variety of being re-hydrated. In all cases, the sporocarps, in groups of

8 . r A e M

N b dark brown, making up half of the total length of the substrates, especially fallen trunks and frequently found on two to 16, appeared very typical, allowing for certain , A 6 a m r C a r I h e c X - sporocarp, continuing as a columella, almost until the apex of feces of herbivores, especially horse and cow, in countries of identification. These data constitute the first record, on a 4 z t E e s i M B o

the sporotheca; the capillitium is very scant, arising from any Europe, Asia, and Africa, with the first record dating to 1876 global scale, of M. vesparia as a coprophilous slime mold. 2 e M A d T S 0 a I point of the columella, made up of purplish brown, thin and in Denmark [11, 10]. Only three of the 62 cultures produced a Typical sporangia of C. violacea were associated with this r d V 1 2 3 4 5 6 7 8 9 10 11 12 13 14 n E

R pale near to the base filaments, ending in short branches, with few sporangia of this species, developing on rabbit feces species and appeared alternately or simultaneously with this Excursions A Figure 2. Number of moist chambers set up and the number of simple or dichotomous branching; spore case dark brown; collected in savanna during the rainy season (July, August) species. positive cultures prepared with feces of rabbit (Sylvilagus spores dark violet-brown, reticulate, 8.16 µm in diameter. The and in the dry season (October), after 12–14 weeks of culture. Examined material: BRAZIL. Sergipe: Areia brasiliensis L.) and horse (Equus caballus L.) collected during 14 field trips (Serra de Itabaiana National Park, Sergipe State, characters found, in the studied material, agree with the Sporangia of P. cinereum were associated with this species. Branca, Serra de Itabaiana National Park, on feces of Brazil). 5 4 3 3 36 REVISTA MEXICANA DE MICOLOGÍA 27, 2008

lower did rodents. This feces moist-chambers deserts percentage was moist-chambers aborted couldresult mean percentage 15% vir chambers other (Figure moist-chambers developed In T

S a m p le s (n º) ime P v ( C Sta c f Fig ginianus the r e e a h a r c comment s b ib 1 1 1 1 1 y b e more p te u of a s 0 2 4 6 8 0 2 4 6 8 authors, b s of a 7.0). r r of a llu

, project it) diversity e a

r r o of

ia B 2). r the sporulation u f s , In ia 3

m

r hare, , . 5 1 a

r

Russia

L acidic plasmodia

: of a z with In 8 of Still, Sp more r Zimmermann, cultures. . b il. C o : ) m b

s sporulation authors which e

r f such fact, H it ic sporulation reported e ib r c 1 2 o u ie cow e r : r m m ( was where prepared m o and this a s A S recent feces (3.8–5.5; c [21]

. r itr y

a r as a in ia Se lv , c r b from thehigh 3 ic was y and p

ila The u obtained, value Stephenson r horse, r s did species the a h and/or r n ia p a

ia a d g herein, . sporulation

,

work of a u

d ( the high (T c pH 6 not n s 4 present h author m e in and with

: c and o

able b is mean e in é C r I white-tailed

r s least sheep, ta r of r sporocarps o cite a o e e higher ib richness. carried percentage b r a s ) the f 5 S obtained a , with the ilie ,

feces a r

, 1). p

m ia a 9 wondered e low 2 [24], work, the r 4 c 4.6) : productive y n n : fact pH levelsfound ia i : substrate e x a s P of C s 6 is o

and 23 than v h pH m o N C of percentage

out io y m who L ten and that a y r s la species, ib tio a a . the Comparing c only ) rabbit (34%) of r tr several e

7 c r in deer u (72%) those te n a e a species ic m set n produced many a a r whether s initial the h l d the ia ,

a substrate,

five o c 7 Pa ,

8 up h b in : and m cultures, o ta in Me obtained m r steppes growing e Odocoileus r ir k of of 129 species in r s plasmodia ic , species e pH a e occurred, all

ta (5.6–8.2; e r u

b of 9 Se positive cultures d o ( the m ilis the tr E

c a moist- r of of , ic f a q horse

g r , r with u high o 1 h ip

low p and 1 u m 3 0 but list the the i 0 a a on by e s : of : in

microenvironmental fermentation the abundance of of other days; feces longer 4, sporulate observed T sporulated most violacea ciner PNSI presented by

able S p o r u l a t io n (d a y s ) a H c ( 2 N L c Fig coprophilous T degradation r f in u : 1 1 2 2 3 3 . e a a able f ) 0 5 0 5 0 5 5 ltu

b 0 0 0 0 0 0 0 0 species, m e tio

eum u m C rabbit, authors of 1). b r a r are abundant itr period e r ir r it) n e n e ib u

d a a 1 ic s dif This groupofor Sporocarps 1) m ,

and l

r b in

4 after p were h h a 4 present, ilis , Pa . on (number r

ferent ia o r :

[5]. the e ia r 48 7 C p r 2 Sp

s process . the authors, of m k Metatrichia. : [12, e a

r the which ,

r ib m of same days); in o

e only myxomycetes. ( The recorded time Se P r d r ic E o species u a h 3 animals,

the two r q la r r 25], w y r , g o but u ia

s tio of ip ith 1 c u a of factors, majority moist-chamber for ten of a 0

s r substrate these e v n could 4 r u :

types

sporocarps)

io some likely p only

f c m Sta Me the e sporulation, a a la c tim ganisms sporulatesinthelast

days b

60% of on e and c t a ta r ( s vesparia such 5 e h results substrate e

o llu e , tr of o a o such

Ar s species,

feces B being e , S be f r ic of s

s pec o u 5 r

of r cyria substrate [3], e only h a 6 f m a : L ) as

ies ia z species, b , , C . as

il. the species ) related b

s cultivation,

corroborate

3 r p v rather C. it of being

8

ib f a : pH. e e 1 for r 7 are even : as s c ( o like ciner : r Cribraria characteristic C p S micr ie m a herbivores. C a A y r to r s 30

lv r ib ia r distinguished r

analyzed 8 i Se c ib than Cribraria a however i noted when r alterations o

y la ea as more ocarpa a , s r r r

f a p r 1

r ia g ia

a r . 1 u , recorded in and m

ia

9

the s : much the

6 continuing d

y

c C m cultivated b : e more days c in x

r o micr P a ic o richness

findings a I m , 10 e n Physarum (horse, h (Figure ta Cribraria m r s r

needed c y a sp., behavior o ili e b y e s tr in a c (Figure ocarpa a lla a c e to for a ic , ia r as e n

11 r other stage u te were ta s p h n 9 is m a a s a the the the the : , 37 on

of of to 3, a 8. 7. 6. 5. 4. 3. 2. 1. in Silva, Parente, Laboratório awarded M. collection Marleno National The authorsthankthemanagementof Angel, Benjamin, Cavalcanti, Barrasa, Alves, Cavalcanti, this Batista, Cavalcanti, F . A. work. and K., M.H., Andréa References Acknowledgements Rickia Botânica Anais Myxomycetes Botânica Brasil. (eds.), Moura, ocorrentes am Comatricha Micologia galináceos Leveduras e Malacitana viven 75. and Revista Fresen. Park, Bezerra J. Costa, A. to D. period; R. Nicola M., L. bi L. fecal C., T L. de K., en L. H., . S.F W Biodiversidade, G. 6: sobre in H., da te Universidade (Zygomycota) Brasileira A.W O. E.V H. Myxomycetes H., icklow .B. 99-1 do do 2002. s for substrates Moreno, Areia Carla da and nas VIII e 1974. Bruna to 6: . Fischman, .S.B. Brasil, Brasil, na outros fungos . Cavalcanti; Mycologia T animais Universidade E.J. materias 17. 1 Poitras, the rufem, CNPq, tu 1 em Regiões Biodiversidade , 1-148. for ra 1975. Reunião Branca, Caldas O de Sampaio, is Santos, cana-de-açúcar Recife, Recife.pp.209-216. 1980. facilities Alves, in

Botânica gênero the cativos, Federal A. 1950. e em a Relationships conservação C. fecales for Norte 42:

Colorado an Milanez, Contribución Productivity fezes Brasil, Nordestina T das fezes de at Bezerra, SE; tr M.I.L. 514-518. An the . and Perichaena for L.M.S. op Recife, no 25: V Rural e UFPE, AlessandraAlencar made e adition de asconcelos, og (2º Nordeste. doctoral to distribuição Recife. their 147-160. pp. to ên herbívoros, grassland. (

V Silva, Saccharum aportación). e I., de ic de ovinos, between Gestinari, the SerradeItabaiana 215-221. 327:1-27. aldineide uso the os to available Clebson de 2002. al technical Pernambuco,

Boletim Fries the estudio sustentável in In no I.M.A. Botânica, biologists grant I.G. : Myxomycete de

Research coprophilous Araújo, Mycologia Táxons Recife, em Br caprinos, suínos, mixomicetos J.M.T officinarum Acta Rocha, Santana as do de Firmino awarded Pernambuco. Pinto, during il assistance hongos Instituto : da PE, . E.L., Sociedade Sociedade de Botanica Carneiro es flora of 67: 1961a. Mucor Brasil. grant pé genus 1985. fungi A.N. and ci the the L.). que 63- em da do to de es

27. 26. T 25. 24. 23. 22. 21. 20. Moreno,G.,J.M.Barrasa,1977.Contribuciónal 19. 18. 17. 16 15. 14. 13. 12. 1 10. 9. 1. Clark, . Ing, Eliasson, Putzke, Mitchell, Lado, W Martin, Novozhilov Farr Stephenson, Keller Stephenson, Schoenlein-Crusius, Eliasson, Maimoni-Rodella, La rufem, icklow do B., , J., M. C., , , Mycological coprorphilous coprófilas. Systematics F Basanta, living temperate Botânica das from soil Ninomiya, Sociedade flora Carneiro A.N. Caspian An Malacitana viven Privately Iowa Pernambuco, J.M.T sustentável Araújo, espécies mixomicetos Consejo Echinosteliales, Cuadernos mite. through the 175-201. (Monograph, N Botaniska 10. brunnea summary Systematics 1994. J., G. 2004. H., .W S. , L., C. e U. D. 2001. D. 2002., o W annotated Fontes . F , , U. t H., D.W W 1976. . Y r Press, Mycologia ., T S. . do The trees, o S. Spiege B., Moura, F Reproductive . ., sobre ., C.J. p . K., Carneiro Nomenmyx. H.W E.L., H., , Lowland. L., Superior V 2002. i , (eds.), 19:7-10. J.C. . Published Ar ocorrentes L., Myxomycetes Brasil. af c . 1984. Phytosociology Notiser P key Botânica forests. Smith, Rickia T a do Moore, Alexopoulos, 3: Flora I.V fected by Iowa. M.F cyria an leaf feeding activities 1989. da . and and rabajo . N. Society

l, Sociedade 16). M. R. em materias A.N. 5-33. Keller checklist Landolt, Ipiranga”, do . to Myxomycetes N I. fungal flora Zemlianskaia, .R. E.V Biodiversidade, litter Geography Geography Liceales, 2004. Mucorales 70:1239- e , Lundqvist, ambientes species, elater C., Universidade Schnittler Neotropica. de 1 w H., 132: Mikologiya Distribution (eds.), 1978. III 1: Flora 1974. Moura, 19 .S.B. Antunes, by do

, Investigaciones , systems 47: A 1999. nas do 53-64. excrement of and Y 2002. 97 Patterns the S.F

Brasil, 551-568. succession. nomenclatural ensis

of o fecales Y Studie Botânica na 51 . Micológica r Brasil. São Dissemination Ef 1969. .K. dung. Regiões k .B. T and author the 1241. Sampaio, of Biodiversidade, 1-530. Região Coprophilous M

, richiales. E.V fect do of of naturais

and Myxomycetes. C. B Biodiversidade and Paulo, Novozhilov yx 1979. - Myxomycetes 1996. Recife.pp. (ingestion-defecation) of New Y T taxonomic Plants Plants M. I s o Inventory of Estado .S.B. and The rufem, Fitopatologiya Mycology (1º om of Federal conservação t . Lado, Universidade Ar a taxonomy of do Schnittler occurrence n Sul incubation Sudeste cyria yc birds in i T ecology Myxomycetes. aportación). Brazil. Científicas, Brasil, c Mucorales Ibérica Fimicolous Sampaio, e 74: 74: ork: Flora ransactions neotro L.M.S. et a taxabase do de antropogênicos l A. es

S.M.M. 87-108. 209-216. 221-223. of stipata Rural , and Myxomycetes: Brasil. observation São G , Or estudio dehongosque 81: J. Estrada-T Micológica Recife.pp. the “Parque , a Revista Myxomycete pical in 16: conservação e New I. ganization of of K.A. r Clark, e Keys on d

temperature e 608-621. Paulo. the Gestinari, Centro-Oeste. uso 37: L.M.S. Federal of e the Myxomycetes 1-222. . Ce de (Zygomycotina) Madrid. n In Karstenia distribuição Malatinsky bark Phytology Acta Myxomycetes. Myxomycetes. , of myxomycetes. Fefelov 53-65.

sustentável ra : myceto Northwestern on University Pernambuco, Araújo, Brasileira D.L. N orres, ti 4. the CD-ROM. om on 217-220. e surface no Gestinari, Ibérica an acarid Rural w for Botanica Espécies Estadual updated Moore, T yx

British , Brasil: J.M.T spores zoans. e on richia 39:1 2003. Flora Y D.W E.L., al 126: , o uso the In es A. de da de de r of of in 2. k - : . . ,

37 Andrade Bezerra, M. F. et al. Coprophilous myxomycetes of Brazil: first report